J. Limnol., 2016; 75(2): 288-296 ORIGINAL ARTICLE DOI: 10.4081/jlimnol.2016.1334

The invasive Chinese pond mussel Sinanodonta woodiana (Lea, 1834) as a host for native symbionts in European waters

Anna CICHY,1 Maria URBAŃSKA,2* Anna MARSZEWSKA,1 Wojciech ANDRZEJEWSKI,3 Elżbieta ŻBIKOWSKA1

1Department of Invertebrate Zoology, Nicolaus Copernicus University, Lwowska 1, 87-100 Toruń; 2Department of Zoology, Institute of Zoology, Poznań University of Life Sciences, Wojska Polskiego 71C, 60-625 Poznań; 3Division of Inland Fisheries and Aquaculture, Institute of Zoology, Poznań University of Life Sciences, Wojska Polskiego 71C, 60-625 Poznań, Poland *Corresponding author: [email protected]

ABSTRACT Biological invasions are commonly observed in both the natural habitats and those which are altered by human activities. An un- derstanding of the mechanisms involved in the successful introduction, establishment and invasion of exotic taxa is essential in predicting of changes in biodiversity and community structure. Symbiont-mediated interactions between exotic and native hosts are of special in- terest due to the indirect effects on population dynamics. The aim of this study was to estimate the presence of symbionts in Chinese pond mussel Sinanodonta woodiana (Lea, 1834), an exotic of mussel in European fresh waters. The number of 340 individuals of S. woodiana was collected from Polish water bodies, including thermally heated lakes and fish pondsonly with natural thermal regime. The examination of mussels revealed the presence of Rhipidocotyle campanula sporocysts and cercariae (Digenea: Bucephalidae), water mites Unionicola ypsilophora (Acari: Hydracarina), oligochaetes Chaetogaster limnaei limnaei (Oligochaeta: Naididae) and chironomids Glyptotendipes sp. (Diptera: Chironomidae). The global prevalence of mussels inhabited by Ch. limnaei limnaei was 7.6%, by water mites and chironomids 3.5%, and by R. campanula cercariae 2.0%. The significantuse difference in the number of mussels with symbionts was identified between heated lakes and fish ponds (χ2=4.15; df=1, P=0.04), with a higher global prevalence of mussels in fish ponds (22.3%) compared to heated lakes (13.7%). R. campanula or U. ypsilophora were only found in mussels collected from ther- mally polluted lakes or fish ponds, respectively. Chironomid larvae and oligochaetes occurred in both types of water bodies. However, Glyptotendipes sp. inhabited mussels with a higher global prevalence in fish ponds than in thermally polluted lakes, while Ch. limnaei limnaei was observed mainly in hosts from heated lakes, and only from one fish pond that were not drained. Our findings indicate that the alien Chinese pond mussel S. woodiana can be inhabited by different groups of symbionts native to Europe, including digenetic trematodes. The results show that S. woodiana can affect directly and indirectly water habitats and the vulnerability of infection with symbionts depends on ecosystem conditions. It occurs that even considerable climate differences do not pose a barrier for exotic mussels to spread.

Key words: Sinanodonta woodiana; Rhipidocotyle; Chaetogaster; Unionicola; Glyptotendipes; Poland.

Received: September 2015. Accepted: December 2015.

INTRODUCTION populations is an important factor facilitating their rapid spread and the increase in their local abundance (Torchin The increasing problem of theNon-commercial spread and colonization et al., 2001; Torchin et al., 2003; Blossey, 2011). of new territories by exotic taxa is of great interest to re- The Chinese pond mussel Sinanodonta woodiana (Lea, searchers due to the direct and indirect impact of exotic 1834) is an alien freshwater bivalve species, which was in- species on native biota. The direct effect, which is usually troduced into European waters in the early 1960s caused by competition between exotic and native species (Kraszewski, 2007). The distribution of S. woodiana in for the same resources, is well documented (Huxel, 1999; Poland in the initial stages of its invasion was restricted to Byers, 2000). The indirect impact is, in turn, linked to artificially heated lakes (Zdanowski, 1996; Spyra et al., modification of complex interactions between exotic and 2012), while the presence of this exotic mussel in waters native organisms and their environment, as exotic species with natural thermal regime was first reported by Bőhme may bring their own symbionts from their native range of (1998) and subsequently by Urbańska et al. (2012). The distribution and/or may acquire native symbionts in new continuously growing number of new localities of S. wood- ranges (Conn et al., 1996; Kelly et al., 2009; Hatcher and iana, as well as the biology and ecology of the species Dunn, 2011; Paterson et al., 2012; Pulkkinen et al., 2013; (Dudgeon and Morton, 1983; Kiss, 1995; Sîrbu et al., 2005; Glodosky and Sandland, 2014; Mori et al., 2015). An Corsi et al., 2007; Du et al., 2011; Douda et al., 2012), in- alien species in new habitats does not usually have natural dicate that this unionid species easily spreads in freshwater enemies and thus the lack of top-down control of their habitats (Andrzejewski et al., 2013). Data on the occurrence A. Cichy et al. 289 of non-parasitic and parasitic symbionts of S. woodiana in inhabiting water bodies of Poland, including thermally its native ecosystems and European water bodies are scanty polluted lakes and fish ponds with natural thermal regime. (Zhao and Tang, 2007; Yuryshynets and Krasutska, 2009; Wu et al., 2012; Yanovich and Shevcuk, 2012) and usually METHODS do not include the diversity of inland waters inhabited by Study area Chinese pond mussel. According to Paterson et al. (2012), several biological and geographical factors are thought to S. woodiana individuals were collected in May and at explain the successful invasion of exotic species and the the beginning of June of 2011 from 8 localities in Poland, acquisition of symbionts, mainly parasites, in invaded including 2 thermally polluted lakes (warm water dis- areas. However, the determinants affecting the acquisition charges from 2 electric power plants) and 6 fish ponds with of native symbionts by exotic hosts remain poorly under- natural thermal regime (Fig. 1). The water from all fish stood, especially in the context of population dynamics of ponds, except for Samita, was regularly drained (Tab. 1). native hosts (Paterson et al., 2012). Thus an important task Long-term drainage took place in autumn and fish ponds now is to look for the possible interactions between S. were refilled with water in early spring next year, whereas woodiana, an exotic mussel native to China, and its native short-term drainage was associated with the exchange of symbionts in Europe. water in autumn within 2 weeks after drainage. The mean The aim of this study was to determine whether and temperature of water in heated lakes during the sampling to what extent S. woodiana can be colonized by symbionts period was nearly 21°C, and was 6°C higher than in the only use

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Fig. 1. Location of study sites in Poland. Fish ponds: 1, Wojnowicki; 2, Czesławicki; 3, Samita; 4, Polna Rzeka; 5, Zaklików; 6, Żary; heated lakes: 7, Gosławskie; 8, Licheńskie. 290 Symbionts of S. woodiana fish ponds under study. The spectrum of ichthyofauna in and of mussels without symbionts between heated lakes heated lakes is diverse and includes at least 14 native and and fish ponds. A Principal Component Analysis (PCA), exotic species (Kapusta et al., 2008; Kapusta and Bo- performed using MVSP 3.22 KCS software, was used to gacka-Kapusta, 2015), while the number of fish species in check for associations of symbiont species with particular the ponds under study ranged from 1 to 3, and only in Wo- types of habitat, i.e. heated lakes or fish ponds. Data were jnowicki Pond it reached 8 species (Tab. 1). log-transformed in order to reduce the impact of particu- larly numerous taxa on results. The term prevalence was Material used for description of one population of hosts inhabited by a symbiont species, while global prevalence was used Chinese pond mussels were gathered by hand in the lit- as a proportion of hosts inhabited by a symbiont species toral zone of the water bodies from a depth of 1.0-1.5 m in relation to all the populations of hosts sampled. and then they were transported to the laboratory in contain- ers under a thin and wet textile. The mean shell dimensions of the collected mussels from both habitat types were com- RESULTS parable: 133.85 (SE 1.54) mm long and 76.94 (SE 1.32) Nearly 17.0% of the 340 collected individuals of S. mm height in heated lakes and 128.04 (SE 2.55) mm long woodiana were inhabited by symbionts belonging to one and 71.23 (SE 1.58) mm height in fish ponds. The number of the 4 systematic groups of invertebrates, including of S. woodiana individuals in the thermally polluted lakes –2 oligochaetes, chironomids, water mites and digenetic exceeds 40 individuals m and the biomass reaches 10 kg trematodes (Fig. 2). Mixed invasions were not observed. m–2, depending on the study sites (Kraszewski and only The symbionts associated with S. woodiana were found Zdanowski, 2001), compared to 19 individuals m–2 and 4.4 in 6 of the 8 localities studied, with prevalence ranging kg m–2 in fish ponds (Spyra et al., 2012). The symbionts in- from 12.0% to 45.4% (Tab. 2). Oligochaetes were the habiting S. woodiana were initially searched for on the most prevalent symbionts of the collected mussels (global mantle surface and between the mantle and the inner side use prevalence of 7.6%; Tab. 2). Hosts inhabited by water of the shell, and next inside the internal organs such as the mites and chironomids occurred less frequently and had gonad, hepatopancreas, gills and heart. Tissue sections were a similar global prevalence of 3.5%, while the cercariae observed under a light microscope (Primostar Carl Zeiss). diagnosed as larvae of R. campanula were noted in 2.0% The species of symbionts were identified on the basis of of the collected mussels. The number of mussels with the morphology of live digenean cercariae (Baturo, 1977; symbionts significantly differed between heated lakes and Richardson, 1990; Taskinen et al., 1991), oligochaetes 2 fish ponds (χ =4,15; df=1, P=0.04). S. woodiana individ- (Kasprzak, 1981; Timm, 1999), chironomids (Wiederholm, uals collected from fish ponds had a higher global preva- 1983) and water mites (Hevers, 1979). The photos of sym- lence (22.3%) than mussels gathered from heated lakes bionts were taken using the Primostar Carl Zeiss micro- (13.7%). PCA analysis showed that samples collected scope and Motic Images Plus 2.0 software. from heated lakes and Samita Pond formed one group and differed from other samples along the first axis due to the Statistical analysis presence of R. campanula and/or Ch. limnaei limnaei A Chi-square test of contingency table was used to (Fig. 3). Along the second axis, samples from one fish compare the numbers of musselsNon-commercial inhabited by symbionts pond (Polna Rzeka) and a heated lake (Gosławskie)

Tab. 1. Characteristics of the study sites. Study sites Coordinates Habitat type Bottom Fish spectrum Wojnowicki 51°56’39”N 16°43’06”E FP (std) Sandy-silty Aa, Ab, Ca, Cy, El, Sg, Sl, Rr Czesławicki 51°29’00”N 17°33’15”E FP (ltd) Silty Cy Samita 52°41’56”N 16°07’11”E FP (nd) Sandy-silty Ca, Cy Polna Rzeka 51°17’16”N 20°25’20”E FP (std) Sandy-loam As, Cy, Li Zaklików 50°45’53”N 22°08’16”E FP (std) Sandy-silty Ci, Cy, Hm Żary 51°19’17”N 15°16’18”E FP (ltd) Sandy-silty Ca, Cy Gosławskie 52°17’17”N 18°14’36”E HL Sandy-silty Aa, Ab, Ca, Cg, Ci, Cy, El, Hm, Hn, Pf, Rr, Sg, Sl, Tt Licheńskie 52°19’24”N 18°20’55”E HL Sandy-silty with a layer of leaves Aa, Ab, As, Ca, Cg, Ci, Cy, El, Hm, Hn, Li, Pf, Rr, Sg, Sl, Tt FP, fish ponds (std, short-term drainage), (ltd, long-term drainage), (nd, not drained); HL, heated lakes. Aa, Anguilla anguilla; Ab, Abramis brama; As, Aspius aspius; Ca, Carassius carassius; Cg, Carassius gibelio; Ci, Ctenopharyngodon idella; Cy, Cyprinus carpio; El, Esox lucius; Hm, Hypoph- thalmichthys molitrix; Hn, Hypophthalmichthys nobilis; Li, Leuciscus idus; Pf, Perca fluviatilis; Rr, Rutilus rutilus; Sg, Silurus glanis; Sl, Stizostedion lucioperca; Tt, Tinca tinca. A. Cichy et al. 291 formed one group, while samples from other water bodies search, R. campanula was found in S. woodiana only in formed another group (Fig. 3). The presence of U. yp- thermally polluted lakes. The ability to create new rela- silophora and/or Glyptotendipes sp. was the factor that tionships in heated lakes may result from both i) the differentiated the samples along the second PCA axis. higher temperature of water, which facilitates the recruit- ment of parasites and promotes their transmission to hosts DISCUSSION (Poulin, 2006); and ii) the more diversified spectrum of the second and final fish hosts of R. campanula, including Interactions between unionid mussels and symbionts Rutilis rutilus, Perca fluviatilis and probably Stizostedion are commonly observed in the environment (Piechocki lucioperca (Gibson et al., 1992), in comparison to fish and Dyduch-Falniowska, 1993). We found 4 groups of in- ponds. In native bivalve species, e.g. A. anatina, the pres- vertebrates occurring on the surface of the mantle and/or ence of bucephalid trematodes decreases the production inside the internal organs of S. woodiana. The presence of glochidia (Taskinien and Valtonen 1995), causes partial of R. campanula in the gonads is the first recorded case or complete castration (Jokela et al., 2005; Gangloff et of occurrence of bucephalid larval stages in S. woodiana al., 2008; Müller et al., 2015), increases mortality (Task- in Poland and probably in Europe. The prevalence of Chi- inen et al., 1997) and causes changes in shell shape nese pond mussels inhabited by R. campanula was com- (Zieritz and Aldridge, 2011). The ecological consequences parable with the results noted by Baturo (1977) and of the infestation of Chinese pond mussels by R. campan- Müller et al. (2015) in native bivalve species (Unio pic- ula remain unknown and further studies should address torum and Anodonta anatina, respectively). In our re- the question of whetheronly this parasite significantly burdens use

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Fig. 2. Symbionts identified in Sinanodonta woodiana. A) Chaetogaster limnaei limnaei; scale bar: 100 µm. B) Glyptotendipes sp.; scale bar: 200 µm. C) Rhipidocotyle campanula; scale bar: 150 µm. D) Unionicola ypsilophora; scale bar: 300 µm. 292 Symbionts of S. woodiana its exotic hosts and thus may limit their spread. The com- namics of native symbionts (Krakau et al., 2006; Thielt- plex interactions between native hosts, exotic hosts and ges et al., 2009; Telfer and Bown, 2012). It is highly prob- native parasites are another interesting issue. The impact able that the presence of R. campanula in S. woodiana of exotic hosts is not associated exclusively with direct decreases the prevalence in native unionids, as the more effects (Douda et al., 2012), as exotic hosts can also indi- diversified spectrum of hosts, the lower prevalence of rectly affect native hosts by altering the population dy- each host species separately. It is suggested that the com-

Tab. 2. Prevalence of S. woodiana inhabited by symbionts in Poland. Study site Type of site No. of collected mussels Prevalence (%) Rc Uy Gl Chl Wojnowicki FP 31 0 16.1 9.7 0 Czesławicki FP 30 0 0 0 0 Samita FP 22 0 13.6 0 31.8 Polna Rzeka FP 12 0 0 41.7 0 Zaklików FP 14 0 28.6 0 0 Żary FP 12 0 0 0 0 Gosławskie HL 44 2.3 0 only 9.1 9.1 Licheńskie HL 175 3.4 0 0 8.6 Total 340 2.0 3.5 3.5 7.6 FP, fish pond; HL, heated lake; Rc, Rhipidocotyle campanula; Uy, Unionicola ypsilophora; Gl, Glyptotendipesuse sp.; Chl, Chaetogaster limnaei limnaei.

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Fig. 3. Principal Component Analysis (PCA) of samples (symbionts inhabiting Sinanodonta woodiana) collected from fish ponds (Wo, Wojnowicki; Za, Zaklików; Pr, Polna Rzeka; Sa, Samita) and heated lakes (Go, Gosławskie; Li, Licheńskie). Chl, Chaetogaster limnaei limnaei; Gl, Glyptotendipes sp.; Uy, Unionicola ypsilophora; Rc, Rhipidocotyle campanula. A. Cichy et al. 293 munity diversity of hosts alters parasite transmission and ronomids Glyptotendipes sp. found during our study were mediates infection parameters, as the presence of other recorded between the mantle and the inner side of S. wood- less competent host species may reduce the prevalence in iana shell. Beedham (1965, 1970, 1971) suggested that the principal host (Telfer et al., 2005; Johnson and Thielt- Glyptotendipes sp. is a facultative parasite of Anodonta ges, 2010; Bouchard et al., 2013). cygnea, as the chironomid larvae fed on the hemocytes and During our research the naidid oligochaete Chaeto- caused the disintegration of the outer mantle epithelium. In gaster limnaei limnaei was also noted. This is turn, Riccardi (1994) indicated that the presence of chirono- commonly observed in molluscs, including bivalves mid larvae in Dreissena polymorpha has no effect on its (Fuller, 1974; Sickel, 1986; Conn et al., 1996) and fresh- condition. The prevalence of Glyptotendipes sp. in the col- water snails (Michelson, 1964; Rodgers et al., 2005; lected samples of S. woodiana was higher in fish ponds Ibrahim, 2007). Previous data reported a different nature with natural thermal regime than in heated lakes. The of the symbiotic relationship between this oligochaete and higher temperature of water in the thermally polluted lakes its bivalve hosts (Eng, 1979; Sickel and Lyles, 1981; Conn can affect the accelerated metamorphosis of the chironomid et al., 1996). Ch. limnaei limnaei, associated with the larva to the imago, which leaves the aquatic environment mantle surfaces of freshwater molluscs, is considered to (Macky, 1977; Stevens, 1998). Moreover, Gudasz et al. be a commensal, and feeds on digenean larvae (Khalil, (2010) found a positive correlation between the temperature 1961; Buse, 1972; Rajasekariah, 1978; Cichy, 2013). Al- of water and the mineralization of organic matter in lake though we found no mixed invasions, it is probable that sediments. A smaller amount of organic matter in the sedi- the relatively high prevalence of S. woodiana inhabited ments of the thermallyonly polluted lakes under study (Brzo- by oligochaetes in heated lakes could be associated with zowska et al., 2007; Bojakowska and Krasuska, 2014), in the presence of R. campanula larvae, one of the sources comparison to reservoirs with natural thermal regime, could of food for oligochaetes. The relationship between Ch. limit food availability and quality for the benthic chirono- limnaei limnaei abundance and cercariae density was ex- mid larvae.use It has been also shown that chironomids living perimentally confirmed by Hopkins et al. (2013). Some in the mantle cavity of mussels were larger than those living authors (Conn et al., 1996) indicate the seasonality of this in the ambient environment (Riccardi, 1994). This confirms annelid species in bivalve hosts and show a positive cor- that bivalve hosts provide better feeding opportunities, in- relation of this phenomenon with water temperature creased mobility, protection from disturbance and reduced changes. According to Sankurathri and Holmes (1976), predation risk (Tokeshi, 1993). Unionicola ypsilophora and the prevalence of Ch. limnaei limnaei decreased in a lake U. intermedia are 2 species commonly observed in mussels at temperatures above 24°C, whereas Poddubnaya (1968) from Europe (Davids, 1973; Baker et al., 1992). In our indicates the optimum temperature for other Chaetogaster study, U. ypsilophora was noted in S. woodiana collected species of about 20°C. In our study the mean temperature from fish ponds only. The presence of the water mites in of water in heated lakes was below 24°C, so the temper- fish ponds, where the high number of chironomids was ature of water probably was not a factor that limited the noted, is not surprising, as unionicolids use the chironomid development of Ch. limnaei limnaei populations. More- larvae as hosts in the life cycle (Baker, 1991). The adult over, the diverse aquatic flora and the longer growing sea- forms of unionicolid water mites are attached to the gills son in the thermally polluted lakes promotes higher of mussels and cause displacement, rupture, and erosion of numbers of ChaetogasterNon-commercialgenerations per year (Learner the gill epithelium (Baker, 1976; Edwards and Vidrine, et al., 1978), which probably contributed to the formation 2006; Fisher et al., 2000; Gangloff et al., 2008). of the association with exotic S. woodiana in these habi- As a large-sized bivalve species expanding its range tats. In addition to both thermally polluted lakes, Ch. lim- of distribution, S. woodiana can be an attractive micro- naei limnaei in S. woodiana was observed in only one fish habitat for various symbionts associated with freshwater pond (Samita). These 3 water bodies formed one group reservoirs. This is possible due to both the biological char- and differed from other samples along the first axis acteristics of the species (large body size and biomass) (PCA). Samita was the only fish pond not drained among and its ecological features (tolerance to water pollution the studied fish ponds. Thus the population of Ch. limnaei and oxygen deficits) (Dudgeon and Morton, 1983; Du et limnaei in mussels was, similarly to lakes, maintained in al., 2011). Some authors emphasize that host density is a the habitat and did not have to rebuild after refilling the key parameter determining the prevalence of hosts pond with water. In the two long-term drained fish ponds (Arneberg et al., 1998; Voutilainen et al., 2009). In our (Czesławicki, Żary) we found no symbionts, which may study, higher density of S. woodiana was noted in heated confirm that habitat disturbance (drainage) influences the lakes (Kraszewski and Zdanowski, 2001; Spyra et al., acquisition of symbionts by hosts. 2012), but higher prevalence of mussels was observed in The association between insects and mussels is not fish ponds. This result suggests that high host density can often observed (Tokeshi, 1993; Riccardi, 1994). The chi- decrease the prevalence of inhabited individuals due to 294 Symbionts of S. woodiana the dilution effect as the probability of an individual host L. inhabited by an insect larva. J. Conch. 26:380-385. being infested by symbionts decreases with increasing Blossey B, 2011. Enemy release hypothesis, p. 193-196. In: D. host density (Mooring and Hart, 1992; Côté and Poulin, Simberloff and M. 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